Large-scale two-photon imaging revealed super-sparse population codes in the V1 superficial layer of awake monkeys

One general principle of sensory information processing is that the brain must optimize efficiency by reducing the number of neurons that process the same information. The sparseness of the sensory representations in a population of neurons reflects the efficiency of the neural code. Here, we employ large-scale two-photon calcium imaging to examine the responses of a large population of neurons within the superficial layers of area V1 with single-cell resolution, while simultaneously presenting a large set of natural visual stimuli, to provide the first direct measure of the population sparseness in awake primates. The results show that only 0.5% of neurons respond strongly to any given natural image — indicating a ten-fold increase in the inferred sparseness over previous measurements. These population activities are nevertheless necessary and sufficient to discriminate visual stimuli with high accuracy, suggesting that the neural code in the primary visual cortex is both super-sparse and highly efficient.

[1]  H. Barlow Critical limiting factors in the design of the eye and visual cortex , 1981 .

[2]  T. Hromádka,et al.  Sparse Representation of Sounds in the Unanesthetized Auditory Cortex , 2008, PLoS biology.

[3]  Matthew R. Krause,et al.  Synaptic and Network Mechanisms of Sparse and Reliable Visual Cortical Activity during Nonclassical Receptive Field Stimulation , 2010, Neuron.

[4]  E T Rolls,et al.  Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. , 1995, Journal of neurophysiology.

[5]  Bruno A. Olshausen,et al.  Highly overcomplete sparse coding , 2013, Electronic Imaging.

[6]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[7]  Jasper Akerboom,et al.  Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging , 2012, The Journal of Neuroscience.

[8]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[9]  P. Lennie The Cost of Cortical Computation , 2003, Current Biology.

[10]  Alexander S. Ecker,et al.  Population code in mouse V1 facilitates read-out of natural scenes through increased sparseness , 2014, Nature Neuroscience.

[11]  H B Barlow,et al.  The Ferrier lecture, 1980 , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[12]  J. Hegdé,et al.  A comparative study of shape representation in macaque visual areas v2 and v4. , 2007, Cerebral cortex.

[13]  Shiming Tang,et al.  Complex Pattern Selectivity in Macaque Primary Visual Cortex Revealed by Large-Scale Two-Photon Imaging , 2018, Current Biology.

[14]  David J. Field,et al.  Emergence of simple-cell receptive field properties by learning a sparse code for natural images , 1996, Nature.

[15]  W. Denk,et al.  Two-photon laser scanning fluorescence microscopy. , 1990, Science.

[16]  James J. DiCarlo,et al.  Balanced Increases in Selectivity and Tolerance Produce Constant Sparseness along the Ventral Visual Stream , 2012, The Journal of Neuroscience.

[17]  B. Willmore,et al.  Sparse coding in striate and extrastriate visual cortex. , 2011, Journal of neurophysiology.

[18]  Martin Rehn,et al.  A network that uses few active neurones to code visual input predicts the diverse shapes of cortical receptive fields , 2007, Journal of Computational Neuroscience.

[19]  J L Gallant,et al.  Sparse coding and decorrelation in primary visual cortex during natural vision. , 2000, Science.

[20]  Fang Liu,et al.  Long-Term Two-Photon Imaging in Awake Macaque Monkey , 2017, Neuron.